Microbial exposure alters HIV-1-induced mucosal CD4+ T cell death pathways Ex vivo

Retrovirology

Volumn 11, Issue 1, 2014, Pages

  Steele, Amanda K ^a   Lee, Eric J ^a   Manuzak, Jennifer A ^a,b   Dillon, Stephanie M ^a   Beckham, John D ^a,b   McCarter, Martin D ^b   Santiago, Mario L ^a,b   Wilson, Cara C ^a,b  

^a UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF COLORADO   (United States)

Author keywords

Human Immunodeficiency Virus; Microbial translocation; Programmed cell death

Indexed keywords

CASPASE 3; CD4 ANTIGEN; CHEMOKINE RECEPTOR CCR5; EFAVIRENZ; GAG PROTEIN; INTERLEUKIN 1BETA CONVERTING ENZYME; LIPOCORTIN 5;

APOPTOSIS; ARTICLE; BYSTANDER EFFECT; CD4 LYMPHOCYTE COUNT; CD4+ T LYMPHOCYTE; CELL AGGREGATION; CELL INTERACTION; CELL VIABILITY; COMMENSAL ESCHERICHIA COLI; ENZYME ACTIVITY; EX VIVO STUDY; FLOW CYTOMETRY; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; HUMAN TISSUE; LAMINA PROPRIA; MONONUCLEAR CELL; NONHUMAN; SIGNAL TRANSDUCTION; T CELL DEPLETION;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1;

APOPTOSIS; CASPASE 1; CD4 LYMPHOCYTE COUNT; CD4-POSITIVE T-LYMPHOCYTES; CELL SURVIVAL; ESCHERICHIA COLI; FLOW CYTOMETRY; HIV-1; HUMANS; IMMUNITY, MUCOSAL; MUCOUS MEMBRANE;

EID: 84896694342     PISSN: None     EISSN: 17424690     Source Type: Journal    
DOI: 10.1186/1742-4690-11-14     Document Type: Article

References (50)

1. Brenchley JM, Schacker TW, Ruff LE, Price DA, Taylor JH, Beilman GJ, Nguyen PL, Khoruts A, Larson M, Haase AT, Douek DC. CD4+ T cell depletion during all stages of HIV disease occurs predominantly in the gastrointestinal tract. J Exp Med 2004, 200:749-759. 10.1084/jem.20040874, 2211962, 15365096.
2. Sankaran S, Guadalupe M, Reay E, George MD, Flamm J, Prindiville T, Dandekar S. Gut mucosal T cell responses and gene expression correlate with protection against disease in long-term HIV-1-infected nonprogressors. Proc Natl Acad Sci U S A 2005, 102:9860-9865. 10.1073/pnas.0503463102, 1159164, 15980151.
3. Chase A, Zhou Y, Siliciano RF. HIV-1-induced depletion of CD4+ T cells in the gut: mechanism and therapeutic implications. Trends Pharmacol Sci 2006, 27:4-7. 10.1016/j.tips.2005.11.005, 16337692.
4. Thomas C. Roadblocks in HIV research: five questions. Nat Med 2009, 15:855-859. 10.1038/nm0809-855, 19661992.
5. Doitsh G, Cavrois M, Lassen KG, Zepeda O, Yang Z, Santiago ML, Hebbeler AM, Greene WC. Abortive HIV infection mediates CD4 T cell depletion and inflammation in human lymphoid tissue. Cell 2010, 143:789-801. 10.1016/j.cell.2010.11.001, 3026834, 21111238.
6. Cooper A, Garcia M, Petrovas C, Yamamoto T, Koup RA, Nabel GJ. HIV-1 causes CD4 cell death through DNA-dependent protein kinase during viral integration. Nature 2013, 498:376-379. 10.1038/nature12274, 23739328.
7. Mattapallil JJ, Douek DC, Hill B, Nishimura Y, Martin M, Roederer M. Massive infection and loss of memory CD4+ T cells in multiple tissues during acute SIV infection. Nature 2005, 434:1093-1097. 10.1038/nature03501, 15793563.
8. Li Q, Duan L, Estes JD, Ma ZM, Rourke T, Wang Y, Reilly C, Carlis J, Miller CJ, Haase AT. Peak SIV replication in resting memory CD4+ T cells depletes gut lamina propria CD4+ T cells. Nature 2005, 434:1148-1152.
9. Kunkel EJ, Boisvert J, Murphy K, Vierra MA, Genovese MC, Wardlaw AJ, Greenberg HB, Hodge MR, Wu L, Butcher EC, Campbell JJ. Expression of the chemokine receptors CCR4, CCR5, and CXCR3 by human tissue-infiltrating lymphocytes. Am J Pathol 2002, 160:347-355. 10.1016/S0002-9440(10)64378-7, 1867126, 11786428.
10. Wilkin TJ, Su Z, Kuritzkes DR, Hughes M, Flexner C, Gross R, Coakley E, Greaves W, Godfrey C, Skolnik PR, et al. HIV type 1 chemokine coreceptor use among antiretroviral-experienced patients screened for a clinical trial of a CCR5 inhibitor: AIDS Clinical Trial Group A5211. Clin Infect Dis 2007, 44:591-595. 10.1086/511035, 17243065.
11. Keele BF, Giorgi EE, Salazar-Gonzalez JF, Decker JM, Pham KT, Salazar MG, Sun C, Grayson T, Wang S, Li H, et al. Identification and characterization of transmitted and early founder virus envelopes in primary HIV-1 infection. Proc Natl Acad Sci U S A 2008, 105:7552-7557. 10.1073/pnas.0802203105, 2387184, 18490657.
12. Smith PM, Garrett WS. The gut microbiota and mucosal T cells. Front Microbiol 2011, 2:111. 3153059, 21833339.
13. Brenchley JM, Paiardini M, Knox KS, Asher AI, Cervasi B, Asher TE, Scheinberg P, Price DA, Hage CA, Kholi LM, et al. Differential Th17 CD4 T-cell depletion in pathogenic and nonpathogenic lentiviral infections. Blood 2008, 112:2826-2835. 10.1182/blood-2008-05-159301, 2556618, 18664624.
14. Ciccone EJ, Read SW, Mannon PJ, Yao MD, Hodge JN, Dewar R, Chairez CL, Proschan MA, Kovacs JA, Sereti I. Cycling of gut mucosal CD4+ T cells decreases after prolonged anti-retroviral therapy and is associated with plasma LPS levels. Mucosal Immunol 2010, 3:172-181. 10.1038/mi.2009.129, 2830855, 19956090.
15. Favre D, Mold J, Hunt PW, Kanwar B, Loke P, Seu L, Barbour JD, Lowe MM, Jayawardene A, Aweeka F, et al. Tryptophan catabolism by indoleamine 2,3-dioxygenase 1 alters the balance of TH17 to regulatory T cells in HIV disease. Sci Transl Med 2010, 2:32. a36.
16. Brenchley JM, Price DA, Schacker TW, Asher TE, Silvestri G, Rao S, Kazzaz Z, Bornstein E, Lambotte O, Altmann D, et al. Microbial translocation is a cause of systemic immune activation in chronic HIV infection. Nat Med 2006, 12:1365-1371.
17. Jiang W, Lederman MM, Hunt P, Sieg SF, Haley K, Rodriguez B, Landay A, Martin J, Sinclair E, Asher AI, et al. Plasma levels of bacterial DNA correlate with immune activation and the magnitude of immune restoration in persons with antiretroviral-treated HIV infection. J Infect Dis 2009, 199:1177-1185. 10.1086/597476, 2728622, 19265479.
18. Pandrea I, Gaufin T, Brenchley JM, Gautam R, Monjure C, Gautam A, Coleman C, Lackner AA, Ribeiro RM, Douek DC, Apetrei C. Cutting edge: experimentally induced immune activation in natural hosts of simian immunodeficiency virus induces significant increases in viral replication and CD4+ T cell depletion. J Immunol 2008, 181:6687-6691. 2695139, 18981083.
19. Estes JD, Harris LD, Klatt NR, Tabb B, Pittaluga S, Paiardini M, Barclay GR, Smedley J, Pung R, Oliveira KM, et al. Damaged intestinal epithelial integrity linked to microbial translocation in pathogenic simian immunodeficiency virus infections. PLoS Pathog 2010, 6:e1001052. 10.1371/journal.ppat.1001052, 2924359, 20808901.
20. Howe R, Dillon S, Rogers L, McCarter M, Kelly C, Gonzalez R, Madinger N, Wilson CC. Evidence for dendritic cell-dependent CD4(+) T helper-1 type responses to commensal bacteria in normal human intestinal lamina propria. Clin Immunol 2009, 131:317-332. 10.1016/j.clim.2008.12.003, 2720400, 19174326.
21. Dillon SM, Manuzak JA, Leone AK, Lee EJ, Rogers LM, McCarter MD, Wilson CC. HIV-1 infection of human intestinal lamina propria CD4+ T cells in vitro is enhanced by exposure to commensal Escherichia coli. J Immunol 2012, 189:885-896. 10.4049/jimmunol.1200681, 3395168, 22689879.
22. Kroemer G, Galluzzi L, Vandenabeele P, Abrams J, Alnemri ES, Baehrecke EH, Blagosklonny MV, El-Deiry WS, Golstein P, Green DR, et al. Classification of cell death: recommendations of the Nomenclature Committee on Cell Death 2009. Cell Death Differ 2009, 16:3-11. 10.1038/cdd.2008.150, 2744427, 18846107.
23. Galluzzi L, Vitale I, Abrams JM, Alnemri ES, Baehrecke EH, Blagosklonny MV, Dawson TM, Dawson VL, El-Deiry WS, Fulda S, et al. Molecular definitions of cell death subroutines: recommendations of the Nomenclature Committee on Cell Death 2012. Cell Death Differ 2012, 19:107-120. 10.1038/cdd.2011.96, 3252826, 21760595.
24. Fink SL, Cookson BT. Apoptosis, pyroptosis, and necrosis: mechanistic description of dead and dying eukaryotic cells. Infect Immun 2005, 73:1907-1916. 10.1128/IAI.73.4.1907-1916.2005, 1087413, 15784530.
25. Silva MT, do Vale A, dos Santos NM. Secondary necrosis in multicellular animals: an outcome of apoptosis with pathogenic implications. Apoptosis 2008, 13:463-482. 10.1007/s10495-008-0187-8, 18322800.
26. Opferman JT, Korsmeyer SJ. Apoptosis in the development and maintenance of the immune system. Nat Immunol 2003, 4:410-415. 10.1038/ni0503-410, 12719730.
27. Alimonti JB, Ball TB, Fowke KR. Mechanisms of CD4+ T lymphocyte cell death in human immunodeficiency virus infection and AIDS. J Gen Virol 2003, 84:1649-1661. 10.1099/vir.0.19110-0, 12810858.
28. Arnoult D, Viollet L, Petit F, Lelievre JD, Estaquier J. HIV-1 triggers mitochondrion death. Mitochondrion 2004, 4:255-269. 10.1016/j.mito.2004.06.010, 16120390.
29. Gougeon ML, Piacentini M. New insights on the role of apoptosis and autophagy in HIV pathogenesis. Apoptosis 2009, 14:501-508. 10.1007/s10495-009-0314-1, 19199038.
30. Miao EA, Rajan JV, Aderem A. Caspase-1-induced pyroptotic cell death. Immunol Rev 2011, 243:206-214. 10.1111/j.1600-065X.2011.01044.x, 3609431, 21884178.
31. Bergsbaken T, Fink SL, Cookson BT. Pyroptosis: host cell death and inflammation. Nat Rev Microbiol 2009, 7:99-109. 10.1038/nrmicro2070, 2910423, 19148178.
32. Al-Sadi R, Ye D, Said HM, Ma TY. Cellular and molecular mechanism of interleukin-1beta modulation of Caco-2 intestinal epithelial tight junction barrier. J Cell Mol Med 2011, 15:970-982. 10.1111/j.1582-4934.2010.01065.x, 20406328.
33. Roselli M, Finamore A, Britti MS, Mengheri E. Probiotic bacteria Bifidobacterium animalis MB5 and Lactobacillus rhamnosus GG protect intestinal Caco-2 cells from the inflammation-associated response induced by enterotoxigenic Escherichia coli K88. Br J Nutr 2006, 95:1177-1184. 10.1079/BJN20051681, 16768842.
34. Scheuring UJ, Sabzevari H, Corbeil J, Theofilopoulos AN. Differential expression profiles of apoptosis-affecting genes in HIV-infected cell lines and patient T cells. AIDS 1999, 13:167-175. 10.1097/00002030-199902040-00004, 10202822.
35. Sloand EM, Kumar PN, Kim S, Chaudhuri A, Weichold FF, Young NS. Human immunodeficiency virus type 1 protease inhibitor modulates activation of peripheral blood CD4(+) T cells and decreases their susceptibility to apoptosis in vitro and in vivo. Blood 1999, 94:1021-1027.
36. Rhee SS, Marsh JW. Human immunodeficiency virus type 1 Nef-induced down-modulation of CD4 is due to rapid internalization and degradation of surface CD4. J Virol 1994, 68:5156-5163. 236459, 8035515.
37. Vanden Berghe T, Vanlangenakker N, Parthoens E, Deckers W, Devos M, Festjens N, Guerin CJ, Brunk UT, Declercq W, Vandenabeele P. Necroptosis, necrosis and secondary necrosis converge on similar cellular disintegration features. Cell Death Differ 2010, 17:922-930. 10.1038/cdd.2009.184, 20010783.
38. Favre D, Lederer S, Kanwar B, Ma ZM, Proll S, Kasakow Z, Mold J, Swainson L, Barbour JD, Baskin CR, et al. Critical loss of the balance between Th17 and T regulatory cell populations in pathogenic SIV infection. PLoS Pathog 2009, 5:e1000295. 10.1371/journal.ppat.1000295, 2635016, 19214220.
39. Gosselin A, Monteiro P, Chomont N, Diaz-Griffero F, Said EA, Fonseca S, Wacleche V, El-Far M, Boulassel MR, Routy JP, et al. Peripheral blood CCR4 + CCR6+ and CXCR3 + CCR6 + CD4+ T cells are highly permissive to HIV-1 infection. J Immunol 2010, 184:1604-1616. 10.4049/jimmunol.0903058, 20042588.
40. Monteiro P, Gosselin A, Wacleche VS, El-Far M, Said EA, Kared H, Grandvaux N, Boulassel MR, Routy JP, Ancuta P. Memory CCR6 + CD4+ T cells are preferential targets for productive HIV type 1 infection regardless of their expression of integrin beta7. J Immunol 2011, 186:4618-4630. 10.4049/jimmunol.1004151, 21398606.
41. Doitsh G, Galloway NL, Geng X, Yang Z, Monroe KM, Zepeda O, Hunt PW, Hatano H, Sowinski S, Munoz-Arias I, Greene WC. Cell death by pyroptosis drives CD4 T-cell depletion in HIV-1 infection. Nature 2013, 505:509-514.
42. Monroe KM, Yang Z, Johnson JR, Geng X, Doitsh G, Krogan NJ, Greene WC. IFI16 DNA sensor is required for death of lymphoid CD4 T cells abortively infected with HIV. Science 2013, 343:428-432.
43. Aziz S, Fackler OT, Meyerhans A, Muller-Lantzsch N, Zeitz M, Schneider T. Replication of M-tropic HIV-1 in activated human intestinal lamina propria lymphocytes is the main reason for increased virus load in the intestinal mucosa. J Acquir Immune Defic Syndr 2005, 38:23-30. 10.1097/00126334-200501010-00005, 15608520.
44. Nazli A, Chan O, Dobson-Belaire WN, Ouellet M, Tremblay MJ, Gray-Owen SD, Arsenault AL, Kaushic C. Exposure to HIV-1 directly impairs mucosal epithelial barrier integrity allowing microbial translocation. PLoS Pathog 2010, 6:e1000852. 10.1371/journal.ppat.1000852, 2851733, 20386714.
45. Fallarino F, Grohmann U, Vacca C, Bianchi R, Orabona C, Spreca A, Fioretti MC, Puccetti P. T cell apoptosis by tryptophan catabolism. Cell Death Differ 2002, 9:1069-1077. 10.1038/sj.cdd.4401073, 12232795.
46. Lee GK, Park HJ, Macleod M, Chandler P, Munn DH, Mellor AL. Tryptophan deprivation sensitizes activated T cells to apoptosis prior to cell division. Immunology 2002, 107:452-460. 10.1046/j.1365-2567.2002.01526.x, 1782830, 12460190.
47. Frleta D, Ochoa CE, Kramer HB, Khan SA, Stacey AR, Borrow P, Kessler BM, Haynes BF, Bhardwaj N. HIV-1 infection-induced apoptotic microparticles inhibit human DCs via CD44. J Clin Invest 2012, 122:4685-4697. 10.1172/JCI64439, 3533550, 23160198.
48. Gasper-Smith N, Crossman DM, Whitesides JF, Mensali N, Ottinger JS, Plonk SG, Moody MA, Ferrari G, Weinhold KJ, Miller SE, et al. Induction of plasma (TRAIL), TNFR-2, Fas ligand, and plasma microparticles after human immunodeficiency virus type 1 (HIV-1) transmission: implications for HIV-1 vaccine design. J Virol 2008, 82:7700-7710. 10.1128/JVI.00605-08, 2493338, 18508902.
49. O'Doherty U, Swiggard WJ, Malim MH. Human immunodeficiency virus type 1 spinoculation enhances infection through virus binding. J Virol 2000, 74:10074-10080. 10.1128/JVI.74.21.10074-10080.2000, 102046, 11024136.
50. Garcia-Calvo M, Peterson EP, Leiting B, Ruel R, Nicholson DW, Thornberry NA. Inhibition of human caspases by peptide-based and macromolecular inhibitors. J Biol Chem 1998, 273:32608-32613. 10.1074/jbc.273.49.32608, 9829999.